Role of food in territoriality and egg production of Buffleheads (Bucephala albeola) and Barrow’s Goldeneyes (Bucephala islandica)
Thompson, Jonathan E
ABSTRACT.-Buffleheads (Bucephala albeola) and the North American population of Barrow’s Goldeneyes (Bucephala islandica) typically breed in boreal and montane regions where food is less available relative to most habitats used by temperate nesting ducks. We investigated diets and digestive organ morphology of sympatrically breeding female Buffleheads and Barrow’s Goldeneyes in central British Columbia. Because those congeners exhibit interspecific aggression in defense of breeding territories, we predicted that competition for food could be a principal factor in evolution of that behavior. We also hypothesized that breeding Buffleheads would show greater variation in digestive organ morphology than Barrow’s Goldeneyes because of their smaller body size and consequently greater reliance on their diet to meet nutritional requirements for egg production. Both species fed predominantly on aquatic insects during all reproductive periods, particularly larvae of damselflies (Zygoptera), midges (Chironomidae), and phantom midges (Chaoborinae). Plant foods, primarily seeds of submergent and emergent vegetation, generally represented
RESUME.–Le Petit parrot (Bucephala albeola) et la population nord-americaine du Garrot d’Islande (Bucephala islandia) nichent generalement dans les regions boreales et montagneuses ou la nourriture est moins disponible comparativement a la plupart des habitats utilises par les canards nichant en milieu tempers. Nous avons etudie l’alimentation et la morphologie des organes digestifs de femelles de Petit parrot et de Garrot d’Islande nichant en sympatrie dans le centre de la Colombie Britannique. Comme ces congeneres montraient des comportements d’agression interspecifiques pour la defense de territoires de nidification, nous avons amis I’hypothese que la competition pour la nourriture pourrait etre le principal facteur dans l’evolution de ce comportement. Nous avons egalement emis l’hypothese que les Petits parrots nicheurs montreraient une plus grande variation dans la morphologie de leurs organes digestifs que les Carrots d’Islande en raison de leur plus petite taille corporelle et, par consequent, de leur plus grande dependance en matiere d’alimentation afin de repondre aux besoins nutritionnels necessaires a la production d’oeufs. Les deux espaces se sont nourries majoritairement d’insectes aquatiques durant touts la periods de reproduction, particulierement de demoiselles (Zigoptera), moucherons (Chironomidae), et Chaoborinae. Les plantes utilisees pour l’alimentation, principalement des graines provenant de vegetation submerges et emergente, representaient
SPECIES IN THE genus Bucephala defend spatially and temporally stable breeding territories from conspecifics and congeners (Savard 1984, 1988; Gauthier and Smith 1987). This differs from other North American ducks in which males typically defend a revolving territory around females from conspecifics (e.g. Mallards [Anas platyrhynchos]; Titman 1983) or no territory at all (e.g. Northern Pintails [Anas acutal; Derrickson 1978). Moreover, Bucephala species typically nest in boreal and montane regions where food is less available than in most other habitats used by breeding ducks in the Nearctic (Patterson 1976). Research on the function of fixed breeding territories in Bucephala has resulted in remarkably diverse conclusions. Donaghey (1975) initially hypothesized that Buffleheads (Bucephala albeola) established breeding territories to defend food for laying females (hereafter the “food defense hypothesis”). In contrast, Gauthier (1987a) suggested that mate-guarding was the primary function of breeding territories in Buffleheads, which secondarily evolved into defense of a specific area rather than a revolving territory around the female to maintain vigilance over their nest site. Thus, Gauthier indicated that the female, rather than food for the female, was the resource defended by a male. Savard and Smith (1987) found that breeding Barrow’s Goldeneyes (Bucephala islandica) were most aggressive toward species that had similar spring and winter diets. Thus, like Donaghey (1975), they speculated that the primary function of territorial behavior in Bucephala was food defense. Subsequently, Savard (1988) suggested that breeding territories may function to reduce interference competition between female goldeneyes and species with similar diets, implying that space rather than food per se was the resource being defended.
We investigated diet composition and digestive organ morphology of female Buffleheads and Barrow’s Goldeneyes relative to stage of reproduction and evaluated interspecific variation in their diets. We predicted that diets of breeding female Buffleheads and goldeneyes would be similar leading to competition for limited food resources in boreal and montane wetlands. Additionally, because smaller species of waterfowl typically store relatively smaller nutrient reserves than large species (Blem 1990, Thompson 1996), smaller species should show greater variation in digestive organ morphology to meet most of their nutritional requirements for egg laying from their diet. Thus, we hypothesized that changes in digestive organ morphology to meet the nutritional demands of reproduction would be more apparent in Buffleheads than in Barrow’s Goldeneyes.
STUDY AREA AND METHODS
Our study area encompassed approximately 250 km^sup 2^ on the Chilcotin Plateau of central British Columbia (52 deg 07’N, 122 deg 27’W approximate center point). Elevations in that region of the Fraser River watershed range from 910 to 1,380 m above sea level. Upland habitats consist of rolling grassland interspersed with mixed stands of aspen (Populus tremuloides), lodgepole pine (Pinus contorta), Douglas fir (Pseudotsuga menziesii), and black spruce (Picea mariana). There are numerous small (
We collected female Buffleheads (n 98) and Barrow’s Goldeneyes (n = 97) at foraging sites (typically observed foraging for >=10 min before collection) or captured them on nests throughout the breeding season in 1993 and 1994. Specimens were collected over a broad range of times (0430 to 2300 PST) to ensure that foods consumed throughout the diel cycle were represented. Generally, we collected no more than two birds of each species from any of the wetlands (n = 137) we studied. We categorized specimens into one of the following reproductive periods: non-Rapid Follicular Growth (non-RFG), prelayers (>=1 rapidly developing ovarian follicle, but no postovulatory follicles), early layers (number of rapidly developing ovarian follicles greater than number of postovulatory follicles), late layers (number of postovulatory follicles greater than number of rapidly developing ovarian follicles), early incubation (15 days incubation). Rapid Follicular Growth was indicated by >=1 developing follicle weighing >=0.14 g (dry mass) in Buffleheads and >=0.17 g (dry mass) in goldeneyes. Non-RFG birds were primarily prebreeders (i.e. birds collected before most birds had initiated RFG), but also included several nonbreeders (i.e. birds with no ovarian growth collected after most birds had initiated RFG). Data from early and late incubating females, most (75%) of which were collected from their nests, were pooled for diet analyses because few of them contained food.
Immediately following collection, we injected 2 to 3 mL of 80% ethanol into the esophagus of each specimen to minimize postmortem digestion (Swanson and Bartonek 1970). We removed esophageal and proventricular contents within 3 to 4 h and placed them into individually labeled vials containing 80% ethanol. In the laboratory, foods were identified, sorted, and oven-dried to constant mass (0.0001 g) at 65 deg C. We identified most invertebrates to family (Merritt and Cummins 1984, Clifford 1991) and plant material to genus (Martin and Uhler 1939, Fassett 1957, Martin and Barkley 1961).
The digestive tract was removed from each specimen and dissected it into the upper digestive tract (i.e. esophagus and proventriculus), gizzard, small intestine, ceca, large intestine, liver, and pancreas. Lengths were measured (1 mm) of the upper digestive tract, small intestine, ceca, and large intestine. Gizzard length (0.01 mm) was measured from the proventricular junction to the most distal point using digital calipers. Unstretched components were measured before removal of ingesta to reduce variation in measurements associated with elasticity of those organs (Thompson and Drobney 1996).
Ingesta and visceral fat were removed from digestive organs before obtaining wet masses. Total digestive tract mass was the summed masses of the upper digestive tract, gizzard, small intestine, ceca, and large intestine. Dry liver mass was determined after extracting lipids as follows. The liver was cut into small pieces, placed in an aluminum drying pan, oven-dried to constant mass at 80 deg C, and then ground to a homogenate using a Moulinex coffee grinder. Cellulose thimbles were filled with ~10 g of dried liver homogenate and subsequently washed with petroleum ether in a modified Soxhlet apparatus to extract lipids (Dobush et al. 1985). We determined lean liver and liver fat mass by extrapolating protein and fat contents of the 10 g sample back to the original dry mass of the liver.
Diets of breeding Buffleheads and Barrow’s Goldeneyes were summarized as aggregate percent dry mass and frequency of occurrence for each food type (Swanson et al. 1974). Small sample sizes for several reproductive periods precluded investigation of annual differences in diet. Therefore, we pooled data from both years for all subsequent analyses. We investigated differences in proportion of plant and animal material and changes in use of specific foods relative to stage of reproduction within each species using Kruskal-Wallis one-way ANOVA (PROC NPAR1WAY; SAS Institute 1985). If we detected differences in use of a specific food or dietary component in the overall model, sequential reproductive periods were compared using Dunns multiple comparisons test (Daniel 1990). We used Mann-Whitney U-tests (PROC NPAR1WAY; SAS Institute 1985) for interspecific comparisons of proportional use of invertebrate taxa and specific plant components.
We investigated variation in digestive organ morphology between reproductive periods and years using two-way ANOVA (PROC GLM; SAS Institute 1985). For digestive organs that differed (P
Seventy-nine of 98 female Buffleheads (81%) contained food in their upper digestive tracts. Buffleheads fed primarily on animal foods, which occurred in all birds and represented >=75% of the dry mass of the diet throughout reproduction (Table 1). Animal foods also represented a larger proportion of the diet (P = 0.046) during laying and incubation than in prior periods (Table 1). Aquatic insects, particularly larvae and pupae of midges (Chironomidae) and phantom midges (Chaoborinae), and damselfly larvae (Zygoptera), composed most of the aggregate dry mass in the diet (Table 1). Despite the diversity of insects consumed, only the proportion of Zygoptera larvae in the diet differed (P = 0.01) between reproductive periods. Buffleheads consumed those insects most frequently during prelaying and incubation (Table 1). Consumption of planorbid snails and unidentified gastropod shell fragments increased (P
Fifty-five of 97 Barrow’s Goldeneyes (57%) contained food in their upper digestive tracts. Animal foods comprised >83% of the diet in non-RFG and breeding female goldeneyes and proportion of animal food in the diet did not vary among reproductive periods (P = 0.1253) (Table 2). Plant foods constituted a smaller proportion of the diet than animal foods (P 0.05) between reproductive periods (Table 2).
Aquatic insects were the predominant food in the diet of breeding female Barrow’s Goldeneyes (Table 2). Zygoptera larvae typically represented the largest fraction of the diet and were most frequently consumed by birds during prelaying, late laying, and incubation (Table 2). Chironomid larvae were the predominant food in the diet of nonbreeding goldeneyes (Table 2), but were generally a smaller proportion of the diet during RFG and incubation. Gastropods were eaten by female Barrow’s Goldeneyes during all periods except non-RFG (Table 2). In most instances, birds consumed fragments of empty gastropod shells, although live planorbid snails were eaten occasionally. Barrow’s Goldeneyes seldom consumed crustaceans (Table 2) despite their abundance in many wetlands used by breeding females. Most plant dry mass in the diet of Barrow’s Goldeneyes consisted of seeds of submergent and emergent macrophytes, particularly those of pondweeds, mare’s tails, and bulrushes (Table 2).
COMPARATIVE DIETS OF BUFFLEHEADS AND BARROW’S GOLDENEYES
Diets of breeding female Buffleheads and Barrow’s Goldeneyes were similar in composition including overall animal and plant content (Table 3). Even when reproductive periods were evaluated separately, there were only two differences in the fractions of animal and plant foods in the diets of those congeners. During prelaying, goldeneyes consumed more animal material (P
Overall, there was more similarity in consumption of specific foods than variation (Table 3). The diet of Buffleheads contained a larger proportion of gastropods (P = 0.001) than did the diet of Barrow’s Goldeneyes, especially during RFG (Tables 1 and 2). Overall consumption of dipterans was similar between species, but Buffleheads consumed proportionately more chaoborinid larvae (P
DIGESTIVE TRACT MORPHOLOGY
Digestive organ morphology of female Barrow’s Goldeneyes did not vary between years (Table 4), but lean liver (P = 0.004) and liver fat (P = 0.045) masses of female Buffleheads were heavier in 1994 than in 1993. For the remaining digestive tract components, years were pooled and variation discussed only in relation to reproductive status (see below).
Total digestive tract mass differed between reproductive periods in Buffleheads (P = 0.001) and Barrow’s Goldeneyes (P = 0.001). In both species, digestive tract mass was heaviest in non-RFG birds and declined (P
Mass of specific digestive organs differed between late laying and early incubation in Buffleheads and Barrow’s Goldeneyes (Table 4), but that variation did not change total digestive tract mass between those periods in either species. Small intestine and lean liver mass decreased (P = 0.05) between late laying and early incubation in Buffleheads, but did not decline (P
Patterns in digestive organ length were similar for female Buffleheads and Barrow’s Goldeneyes (Table 4); the longest small intestine lengths occurred prior to RFG and during late laying followed by a sharp decline (P
Bufflehead diet.-Breeding female Buffleheads consumed primarily aquatic insects, particularly larvae of chironomids, chaoborinids, and damselflies. Likewise, Munro (1942) found that Buffleheads breeding in the southern interior of British Columbia fed principally on aquatic insects, but reported that odonate larvae and corixids were the primary insects in their diet. Importance of soft-bodied dipteran larvae was likely underestimated by Munro (1942) because his data were based primarily on gizzard contents (see Swanson and Bartonek 1970). Erskine (1972) also indicated that insects were predominant in the diet of adult Buffleheads during spring and summer; birds ate principally chironomid larvae during spring, but consumed more odonates and corixids during summer. Based on examination of combined esophageal and gizzard contents, Erskine (1972) indicated that corixids were eaten by 36% of Buffleheads during spring and 65% of birds during summer. Based exclusively on esophageal contents, hemipterans, including both corixids and notonectids, were not frequently ingested by female Buffleheads breeding on the Chilcotin Plateau. All studies (Munro 1942, Erskine 1972, this study), regardless of analytical approach or geographic location, have found that odonate larvae ranked either first or second in dietary importance to breeding Buffleheads.
Compared with other Bucephala, Buffleheads consume more gastropods throughout their annual cycle, particularly planorbid and lymnaed snails during breeding season when birds are using freshwater habitats (Cottam 1939, Erskine 1972). We found that consumption of gastropods and their shell fragments exceeded 25% of the diet of female Buffleheads during late laying (Table 1) when birds were incurring high mineral requirements for eggshell production. Gastropod shell fragments were consumed more frequently than live gastropods, suggesting that Buffleheads consumed them primarily for their mineral content. Crustaceans were a small proportion (
Barrow’s Goldeneye diet.-Breeding female Barrow’s Goldeneyes also principally consumed aquatic insects, particularly zygoptera larvae and larvae and pupae of chironomids and chaoborinids. Munro (1939) reported that Barrow’s Goldeneyes breeding in southern British Columbia frequently fed on odonate larvae and hemipterans, but he likely overestimated consumption of hemipterans and underestimated the importance of soft-bodied insects (see above). Bengston (1971) reported that breeding females from the Icelandic population of Barrow’s Goldeneyes fed principally on chironomid larvae and lymnaed snails. He found that consumption of chironomid larvae increased as summer progressed, whereas use of gastropods (specifically Lymnaea spp.) decreased. In British Columbia, the trend was the opposite; consumption of chironomid larvae decreased and ingestion of gastropods increased as the breeding season progressed (Table 2).
Gastropods were not consumed by goldeneyes until RFG and constituted
Plant foods represented
Comparison of diets.-Diets of Buffleheads and Barrow’s Goldeneyes showed considerable overlap in both foods consumed and proportion of the diet that those foods represented. Their diets were most alike during non-RFG when birds were establishing breeding territories. Therefore, if interspecific aggression is related to defense of foods, it should be most common shortly after birds arrive on breeding areas. Furthermore, the few interspecific differences in diets were likely due to interacting factors of body size and nutritional requirements during egg production and variation in food availability between wetlands rather than adaptations to reduce interspecific competition.
Our data on diets of breeding Buffleheads and Barrow’s Goldeneyes cast doubt on Gauthier’s (1987a) conclusion that food defense was not a function of territoriality in Bucephala. His test of the food defense hypothesis was flawed because he assumed that Buffleheads fed predominantly on nektonic invertebrates. We found that Buffleheads and Barrow’s Goldeneyes fed primarily on benthic insects and gastropods. It is thus not surprising that Gauthier (1987a) found no correlation between territory size and nektonic food density or a relation between reproductive success and food abundance. Furthermore, Gauthier’s conclusion that mate guarding is the primary function of territorial behavior in Bucephala is inconsistent with the fact that forced copulation has never been observed in that genus (see review in Savard 1988). It is also inconsistent with evidence that many Bucephala exhibit long term monogamy (Savard 1985, Gauthier 1987b), and with DNA fingerprinting studies that have found no mixed paternity in unparasitized goldeneye clutches (Eadie et al. 1995). Furthermore, protection of paternity does not explain why male Bucephala exclude conspecific females and subadults, congeners, and other species with similar diets from their territories. Protection of paternity also does not explain why territories are not centered around females (Donaghey 1975, Savard and Smith 1987), nor why males defend breeding territories when the female is absent. Finally, it is highly unlikely that nest site protection resulted in evolution of fixed territories, because there is little evidence that male Bucephala protect the nest site. In fact, several female Bucephala may nest in a single tree if separate nest cavities are available, and breeding territories are often not adjacent to the nest site (J. E. Thompson pers. obs.). Additional studies are needed to test hypotheses on the evolution of territoriality in Bucephala, but we suggest that given the relatively unproductive breeding habitats and ephemeral and patchy nature of foods used by Buffleheads and goldeneyes, the food defense hypothesis is the most parsimonious explanation for intraspecific and interspecific territorial behavior in those species.
Digestive organ morphology.-Female Buffleheads and Barrow’s Goldeneyes arrived on breeding areas with relatively heavy digestive tracts, especially muscular gizzards, which are essential to process marine mollusks and crustaceans that constitute most of their diet during winter (Hirsch 1980, Koehl et al. 1982, Vermeer 1982). Large digestive organs may also have resulted from hyperphagia to store somatic nutrients during spring migration. Gizzard and ceca mass of Buffleheads and goldeneyes declined rapidly on breeding areas as birds began feeding on aquatic insects. Such declines are consistent with those observed in other ducks (Miller 1975, Kehoe and Ankney 1985) when they feed on highly digestible foods. The gizzard can be an important source of somatic protein for clutch formation in waterfowl (Ankney 1977, Korschgen 1977, Raveling 1979, Krapu 1981), but gizzard mass was stable during laying in Buffleheads and Barrow’s Goldeneyes indicating that this muscle was not a significant source of protein for egg production. However, catabolized gizzard tissue may have been used to facilitate growth of the oviduct prior to egg laying.
Digestive organ morphology of Barrow’s Goldeneyes remained relatively constant during RFG, but digestive organs of Buffleheads showed changes consistent with their greater dependency on exogenous nutrients during egg formation. Small intestine length of Buffleheads increased during late laying, which may have improved chemical digestion and increased nutrient absorption when Buffleheads were probably most dependent on dietary nutrients (Miller 1975). Pancreas mass in Buffleheads increased during early laying probably to enhance production of digestive enzymes in response to intensive foraging during egg synthesis.
Daily food intake and digestive organ mass typically decline with decreased time spent foraging during incubation (Drobney 1984, Afton and Paulus 1992). During early incubation, mass and length of the small intestine and lean mass of the liver decreased in Buffleheads and Barrow’s Goldeneyes. Also, mass of the upper digestive tract and pancreas declined with onset of incubation in Buffleheads. Atrophy of the digestive tract in incubating Buffleheads and Barrow’s Goldeneyes would reduce metabolic energy requirements (Moss 1974) permitting increased incubation constancy and potentially enhancing nest success. Only ceca mass in Barrow’s Goldeneyes increased during incubation, which likely was related to the slight increase in consumption of more fibrous plant material (Duke 1986). Buffleheads did not undergo a similar change in cecal mass because their diet consisted almost exclusively of aquatic insects during incubation.
Exogenous nutrients and egg production.-Buffleheads and Barrow’s Goldeneyes apparently obtain a large fraction of their prebreeding lipid reserves by feeding on fish eggs during spring migration (Vermeer 1982). Female Buffleheads acquired all of the protein required for clutch formation by consuming aquatic invertebrates on breeding areas (Thompson 1996). Similarly, Barrow’s Goldeneyes acquired clutch protein exclusively from their diet in 1994, and only catabolized a small amount of endogenous protein to meet clutch protein requirements in 1993 (Thompson 1996). Insects are an excellent source of protein and lipids for producing eggs because of their efficient conversion to albumen and yolk (Krapu and Reinecke 1992). Some calcium for eggshell production originated from catabolism of somatic minerals in both species during the 1993 breeding season (Thompson 1996), but most mineral requirements were met by consumption of gastropods, gastropod shell fragments, and possibly other invertebrates. Furthermore, Buffleheads occasionally consumed avian eggshell fragments and small bones as additional sources of calcium.
The digestive organs of breeding female Buffleheads exhibited more variation than that of female Barrow’s Goldeneyes, which was consistent with our hypothesis that smaller species of waterfowl should show greater modification in gut morphology than do larger species to meet their nutritional demands for reproduction. An apparent example of the interaction between body size and nutritional demands for egg production is the higher proportional consumption of gastropods by Buffleheads when mineral requirements for eggshell production were elevated during laying. Smaller body size apparently limits the potential contribution of somatic mineral to eggshell synthesis in Buffleheads (Thompson 1996), and thus requires females to ingest more calcareous foods and have the ability to assimiliate those nutrients. Nutrient storage is less constrained by body size in Barrow’s Goldeneyes than in Buffleheads, because goldeneyes are over twice as large. Larger body size allows them to maintain and use relatively larger nutrient reserves and consequently reduce their reliance on exogenous nutrients during clutch formation.
Primary research funding for this project was provided by the Natural Science and Engineering Research Council of Canada through an operating grant awarded to C.D.A. Academic year support for J.E.T. was provided through several sources including an Ontario Graduate Scholarship and University of Western Ontario Graduate Research Fellowship. This research was facilitated by generous cooperation and logistical support provided by Murray Clarke, Brad Arner, Doug Regier, and Ed Herman of Ducks Unlimited Canada, and Andre Breault and Doug Dockerty of the Canadian Wildlife Service. Permission to work in portions of the study area was kindly granted by the Canadian Department of National Defense (Chilcotin Military Training Area) and Brian Durrell of the Wine Glass Ranch. Dedicated field and lab assistance for this project was provided by Trevor Matthews, Sarah Lee, and Steve Timmermans. Finally, we would like to thank Jim Sedinger and Jack Millar for their insightful comments on earlier drafts of this manuscript and Ronald Drobney and Jean-Pierre Savard for their thorough reviews.
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JONATHAN E. THOMPSON1 AND C. DAVISON ANKNEY
Ecology and Evolution Group Department of Zoology, University of Western Ontario, London, Ontario N6A 5B7, Canada
1Present address: Ducks Unlimited Canada, #200, 10720-178 Street, Edmonton, Alberta T5S 1J3, Canada.
Associate Editor: L. Smith
Copyright American Ornithologists’ Union Oct 2002
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